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Reticularis thalami afferents to the ventrobasal complex of the rat thalamus: an electron microscope study
Brain Research, 270 (1983) 325-329
325
Elsevier
Reticularis thalami afferents to the ventrobasal complex of the rat thalamus: an electron microscope study MARC PESCHANSKP, HENRY J. RALSTON2and FRAN(~OISEROUDIER l I UnitO de recherches de neurophysiologie pharmacologique, INSERM U 161, 2 rue d'AlOsia 75014, Paris (France), and 2Department of Anatomy, UCSF, Medical School, San Francisco 94143, CA (USA)
(Accepted March 15th, 1983) Key words: nucleus reticularis thalami - - ventrobasal complex- - electron microscopy- - kainic acid
Afferents from the nucleus reticularis thalami (RT) to the thalamic ventrobasal complex were studied in the rat by looking for degenerating terminals after selective neurotoxic lesion of RT using injections of kainic acid. Several lines of evidence are presented indicating that RT afferents terminate in the VB by F type (Gray type II) terminals and that F type terminals in the VB all depend of RT neurons. The thalamic ventrobasal complex (VB) of the rat contains 3 major types of synaptic terminals: (1) large L-type terminals (about 2-4 ~m in diameter), containing numerous mitochondria and round vesicles, which contact cell bodies and large dendrites (see Fig. 3) by asymmetrical synapses; (2) small S-type terminals (about 1 ktm in diameter), containing at the most one mitochondrion and round vesicles, which make asymmetrical synapses with thin dendrites (see Fig. 3); and (3) F-type terminals of intermediate size (about 1-2 ~m in diameter), containing 1-3 mitochondria and flattened vesicles, and making symmetrical (Gray-type II) synapses with dendrites of all sizes and with cell bodies4, 8A7. This relatively simple organization has been further defined by the demonstration that cortico-thalamic afferents terminate only in S-type terminals and that afferents from the spinal cord and the dorsal column nuclei have L-type terminals (see refs. in refs. 4 and 8). In contrast, the origin of F-type terminals remains unclear. Two studies dealing with afferents from the nucleus reticularis thalami (RT) to the dorsal lateral geniculate nucleus 11,13 found that F-type terminals arose, in part, from RT neurons. Since RT is a homogeneous structure (see below) and in addition projects to VB3AO it is suggested that at least some F terminals in VB may be associated with RT afferents. It is very difficult to demonstrate this projection using autoradiographic techniques or electrolytic le0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
sions since the portion of RT related to the VB is too thin (200/~m wide at the most) and has a sheet-like shape, and because the nucleus is crossed by numerous fibers from various origins, lesions of which could complicate the interpretation of the data. Recently it has been shown, however, that extensive neuronal loss could be induced in RT by remote injections of kainic acid (KA) in other diencephalic structures 15. Using this technique, we have sought in the present study to define more precisely the ultrastructural features of RT afferents to VB by looking for degenerating profiles following KA injection. A total of 15 rats anesthetized with chloral hydrate (400 mg/kg) intraperitoneally, received a slow pressure injection of 3-10 nmol of KA (0.1-0.3 ~1 in water, 20 min) using a 1 ,ul Hamilton syringe in the ventral part of the striaturn, close to the internal capsule (AP 6; L 4.5; D 4 according to the atlas of Albe-Fessard et al. l). After survival times of 1-i0 days the animals received an overdose of Nembutal and were perfused intracardially with heparinized buffered saline (pH 7.4) at 37 °C followed by a solution containing 1% paraformaldehyde, 3% glutaraldehyde, 4% sucrose in 0.1 M phosphate buffer (pH 7.4) at 4 °C. Sections of 100gm thickness were cut on a Vibratome (Oxford Instruments) and every other section osmicated, dehydrated and embedded in Epon-araldite. The VB was then trimmed out carefully from the plastic embedded slices prior to final sectioning for electron mi-
326
Fig. 1A: Low power photomicrograph (34 × ) showing the degeneration in the nucleus reticularis thalami (rt) after an injection of kainic acid (star) at the border between the internal capsule (ic) and the striatum. Note the replacement of RT neurons by glial cells; normal VB neuronal somas are well spaced in the nucleus. Survival time, 10 days. B: photomicrograph of the same field of the contralateral (unlesioned) side. Fig. 2. Electron photomicrograph of a degenerating myelinated axon in VB (17,000 x ). Survival time, 2 days. Fig. 3. Low power electron photomicrograph (5610 x ) of a portion of the medial VB. Survival time, 1 day. Degenerating profiles (d) appear shrunken and electron dense. They contact dendrites of different sizes. At the bottom right, both a normal L-type terminal and a degenerating profile (arrowhead d) contact the same large dendrite.
327 croscopy. Thin sections were stained with uranyl acetate and lead citrate. The n o n - o s m i c a t e d alternate sections were m o u n t e d and counterstained with cresyl violet to permit a light microscopic analysis of the degeneration. In two cases, rats received i o n t o p h o retic applications of horseradish p e r o x i d a s e (50% in water) in the VB and in the s o m a t o s e n s o r y cortex, respectively. In these two cases, non-osmicated sections were submitted to M e s u l a m ' s H R P histochemical technique 9 using 3 , 3 ' , 5 , 5 ' - t e t r a m e t h y l b e n z i d i n e as a c h r o m o g e n , before final mounting and counterstaining with carmine. Out of the 15 rats, 7 were discarded because the diffusion of K A led to a neuronal loss not only in R T but also in VB. In general, injections larger than 0.1 /~l over 20 min ( a p p r o x i m a t e l y 3 nmol of K A ) diffused to VB and rapid injections, even of the lowest quantity, also led to a large lesion. Survival time
seemed to have little influence upon the extent of the lesion. Indeed, as shown in Fig. 1, 10 days after the injection, degeneration could be restricted to R T which is then completely filled with reactive glial cells while VB exhibit apparently normal neurons. These data are in agreement with those of Peterson and Moore is who pointed out the selective effects of K A on diencephalic neurons, especially in RT. H o w e v e r , using striatal injection sites, little if any d e g e n e r a t i o n was observed in other ventral thalamic structures (zona incerta, subthalamus and ventral lateral geniculate nucleus) which were destroyed after more caudal injections. Cortico-thalamic and thalamo-cortical pathways cross the R T and the lack of a lesion of both these pathways was checked using control injections of horseradish peroxidase. They confirmed that cortical and VB neurons could be retrogradely filled after in-
Fig. 4. Electron photomicrograph (24.700 ×) of a degenerated terminal with relative preservation of the membranes bordering a synaptic cleft (arrow). At the bottom left, the inset shows a higher magnification photomicrograph (47,500 x) of the same synaptic arrangement. Note the presence of a densification of the postsynaptic membrane without a postsynaptic density and the existence of numerous swollen vesicles in the electron-dense cytoplasm of the degenerating terminal. Survival time, 1 day.
328 jections in VB and in the somatosensory cortex respectively; in contrast, no R T neurons were labeled after VB injection. Tissue from the 8 remaining animals was studied with the electron microscope and degenerating profiles were found in 5 animals which had survived 24-72 h after injection. The 3 others had survived longer times (5, 7 and 10 days) and did not show degenerating terminal profiles. In the first 5 rats, degenerating myelinated axons (Fig. 2) and terminal profiles (Figs. 3 and 4) were observed throughout the VB. These latter appeared as shrunken terminals with a very irregular outline and were filled with electron dense cytoplasm. Although in such electron dense terminals vesicles are generally swollen and their shape cannot be recognized, several lines of evidence indicate that these terminals are mostly Ftypes: for example the synaptic contact, when preserved, did not exhibit a post-synaptic density (Fig. 4 arrowhead) which indicates a symmetrical (Graytype II) synapse, typical of F type terminals in the rat VB. Degenerating terminals were observed in contact with both large (Fig. 3, bottom right) and thin (Fig. 4) dendrites as well as with somas. Such a widespread variation of contacts is also typical of F-type terminals in the rat VBS,8, ~4. Lastly, no normal F terminals could be seen in the survey of tissue from the 3 animals which survived more than 3 days after the injection. This can be interpreted as the result of the elimination of the degenerated profiles through macrophagic activity. The results of the present study, based on the specific neurotoxic lesion of R T by kainic acid injection indicate that F terminals are associated in the VB with afferents from RT. These results are in agreement with those obtained from studying degenerating terminals in the dorsal lateral geniculate nu-
cleus after either an electrolytic lesion of the R T area 13 or labeled profiles after injection of tritiated amino acid in R T u. A notable point of difference in these studies is the observation that in VB terminals making symmetrical synapses seem to depend completely of R T axons while in the geniculate nucleus, terminals containing pleiomorphic vesicles have been identified 6 which are not labeled after RT lesion or injection. This difference is, however, in agreement with the hypothesis that these 'pleiomorphic' terminals depend on intrinsic (Golgi-type II) neurons since such neurons have been described in the geniculate nucleus (see Discussion in ref. 11) but not in the VB of the rat4,~6,is. Such a similarity in ultrastructural morphology was expected, due to the striking homogeneity exhibited by R T neurons. Indeed all studies of R T neurons indicate that these neurons all project from R T to diencephalic and tectal structures 3, that they exert a comparable inhibitory action upon the various thalamic units ~9 and that they all contain G A B A a and somatostatin 12.
1 Albe-Fessard, D., Stutinski, F. and Libouban, S., Atlas stOr(otaxique du dienc~phale du rat blanc, C NRS, Paris, 1966. 2 Houser, C. R., Vaughn, J. E., Barber, R. P. and Roberts, E., GABA neurons are the major cell type of the nucleus cell type of the nucleus reticularis thalami, Brain Research, 200 (1980) 341-354. 3 Jones, E. G., Some aspects of the organization of the thalamic reticular complex. J. comp. Neurol., 162 (1975) 285-308. 4 Lee, C. L., The Structural Organization of the Rat Ventro-
basal Complex, PhD. Thesis , Univ. California, Berkeley,
The present results are interesting in that they demonstrate at the ultrastructural level that it is possible to destroy an entire synaptic population and thus to disrupt totally the effects exerted by R T neurons upon thalamic neuronal functioning. The effects on G A B A and somatostatin concentrations of such a disruption and the electrophysiological consequences on the VB neuronal activity are presently under study. The authors are greatly indebted to Dr. D. D. Ralston for the review of the manuscript and to Miss Hoch for secretarial assistance. They also wish to thank the members of the SCN 18 of I N S E R M (Dr. Bouteille) for their skillful technical assistance.
1981. 5 Lee, C. L., Peschanski, M. and Ralston, H. J. III, Morphophysiology of neurons of the rat ventrobasal thalamic complex. An intracellular HRP study, Pain, Suppl. 1 (1981) S 210. 6 Lenkov, D. N., Winkelmann, E., Braver, K. and Bruckner, G., Vesicle size in basic classes of synapses in the rat's lateral geniculate nucleus, J. Hirnforsch., 19 (1978) 415-42l. 7 Lieberman, A. R. and Webster, K. E., Aspects of the syn-
329
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11
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13
aptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. An u[trastructural study of the normal and of the experimentally deafferented nucleus of the rat. J. Neurophvsiol., 3 (1911) 677-710. MacAllister. J. P. and Wells, J.. The structural organization of the ventral posterolateral nucleus in the rat, J. comp. Neurol.. i97 ( 1981 ) 271-301. Mesulam. M. M., Tetramethyl benzidine for horseradish peroxidase neurohistochemistry. A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and effcrents, J. Histochem. Cytochem., 26 (1978) 106-117. Minderhood, J. M., An anatomical study of the efferent connections of the thalamic reticular nucleus, Exp. Brain Res.. 12 (1971) 435-446. Montero. V. M. and Scott, G. L., Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study, Neuroscience, 6 (1981) 2561-2578. Oertel, W., Graybiel, A. M,, Mugnaini, E., Elde, R., Schmechel, D. and Kopin. I., Coexistence of glutamate decarboxylase immunoreactivity and somatostatin-like immunoreactivity in neurons of nucleus reticularis thalami of the cat, Neurosci., Abstr., 7 (1981) 223. Ohara, P. T., Sefton. A. J. and Lieberman, A. R., Mode of
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termination of afferents from the thalamic reticular nucleus of the rat, Brain Research, 197, (1980) 503-506. Peschanski, M., Lee, C. L. and Ralston, H. J. Ill, Neurons of the rat ventrobasal thalamic complex responsive to stimuli applied to the face or to the limbs. An intracellular HRP study with electron microscopy, Neurosci. Lett., Suppl. 7 (1981) S 136. Peterson, G. M. and Moore, R. Y., Selective effects of kainic acid on diencephalic neurons, Brain Research, 202 (1980) 165-182. Ralston, H. J. llI, The neuronal and synaptic organization of the ventrobasal thalamus in rat, cat and monkey. In G. Macchi (Ed.), The Somatosensory Thalamus, Elsevier, Amsterdam, in press. Tripp, L. N. and Wells, J., Formation of new synaptic terminals in the somatosensory thalamus of the rat after lesions of the dorsal column nuclei, Brain Research, 155 (1978) 362-367. Wells, J., Mathews, T. J. and Ariano, M A., Are there interneurons in the thalamic somatosensory projection nucleus in the rat?, Soc. Neurosci. Abstr., 8 (1982) 37. Yingling, C. D. and Skinner, J. E., Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami, Electroenceph. clin. Neurophysiol., 41 (1976)476-482.
325
Elsevier
Reticularis thalami afferents to the ventrobasal complex of the rat thalamus: an electron microscope study MARC PESCHANSKP, HENRY J. RALSTON2and FRAN(~OISEROUDIER l I UnitO de recherches de neurophysiologie pharmacologique, INSERM U 161, 2 rue d'AlOsia 75014, Paris (France), and 2Department of Anatomy, UCSF, Medical School, San Francisco 94143, CA (USA)
(Accepted March 15th, 1983) Key words: nucleus reticularis thalami - - ventrobasal complex- - electron microscopy- - kainic acid
Afferents from the nucleus reticularis thalami (RT) to the thalamic ventrobasal complex were studied in the rat by looking for degenerating terminals after selective neurotoxic lesion of RT using injections of kainic acid. Several lines of evidence are presented indicating that RT afferents terminate in the VB by F type (Gray type II) terminals and that F type terminals in the VB all depend of RT neurons. The thalamic ventrobasal complex (VB) of the rat contains 3 major types of synaptic terminals: (1) large L-type terminals (about 2-4 ~m in diameter), containing numerous mitochondria and round vesicles, which contact cell bodies and large dendrites (see Fig. 3) by asymmetrical synapses; (2) small S-type terminals (about 1 ktm in diameter), containing at the most one mitochondrion and round vesicles, which make asymmetrical synapses with thin dendrites (see Fig. 3); and (3) F-type terminals of intermediate size (about 1-2 ~m in diameter), containing 1-3 mitochondria and flattened vesicles, and making symmetrical (Gray-type II) synapses with dendrites of all sizes and with cell bodies4, 8A7. This relatively simple organization has been further defined by the demonstration that cortico-thalamic afferents terminate only in S-type terminals and that afferents from the spinal cord and the dorsal column nuclei have L-type terminals (see refs. in refs. 4 and 8). In contrast, the origin of F-type terminals remains unclear. Two studies dealing with afferents from the nucleus reticularis thalami (RT) to the dorsal lateral geniculate nucleus 11,13 found that F-type terminals arose, in part, from RT neurons. Since RT is a homogeneous structure (see below) and in addition projects to VB3AO it is suggested that at least some F terminals in VB may be associated with RT afferents. It is very difficult to demonstrate this projection using autoradiographic techniques or electrolytic le0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
sions since the portion of RT related to the VB is too thin (200/~m wide at the most) and has a sheet-like shape, and because the nucleus is crossed by numerous fibers from various origins, lesions of which could complicate the interpretation of the data. Recently it has been shown, however, that extensive neuronal loss could be induced in RT by remote injections of kainic acid (KA) in other diencephalic structures 15. Using this technique, we have sought in the present study to define more precisely the ultrastructural features of RT afferents to VB by looking for degenerating profiles following KA injection. A total of 15 rats anesthetized with chloral hydrate (400 mg/kg) intraperitoneally, received a slow pressure injection of 3-10 nmol of KA (0.1-0.3 ~1 in water, 20 min) using a 1 ,ul Hamilton syringe in the ventral part of the striaturn, close to the internal capsule (AP 6; L 4.5; D 4 according to the atlas of Albe-Fessard et al. l). After survival times of 1-i0 days the animals received an overdose of Nembutal and were perfused intracardially with heparinized buffered saline (pH 7.4) at 37 °C followed by a solution containing 1% paraformaldehyde, 3% glutaraldehyde, 4% sucrose in 0.1 M phosphate buffer (pH 7.4) at 4 °C. Sections of 100gm thickness were cut on a Vibratome (Oxford Instruments) and every other section osmicated, dehydrated and embedded in Epon-araldite. The VB was then trimmed out carefully from the plastic embedded slices prior to final sectioning for electron mi-
326
Fig. 1A: Low power photomicrograph (34 × ) showing the degeneration in the nucleus reticularis thalami (rt) after an injection of kainic acid (star) at the border between the internal capsule (ic) and the striatum. Note the replacement of RT neurons by glial cells; normal VB neuronal somas are well spaced in the nucleus. Survival time, 10 days. B: photomicrograph of the same field of the contralateral (unlesioned) side. Fig. 2. Electron photomicrograph of a degenerating myelinated axon in VB (17,000 x ). Survival time, 2 days. Fig. 3. Low power electron photomicrograph (5610 x ) of a portion of the medial VB. Survival time, 1 day. Degenerating profiles (d) appear shrunken and electron dense. They contact dendrites of different sizes. At the bottom right, both a normal L-type terminal and a degenerating profile (arrowhead d) contact the same large dendrite.
327 croscopy. Thin sections were stained with uranyl acetate and lead citrate. The n o n - o s m i c a t e d alternate sections were m o u n t e d and counterstained with cresyl violet to permit a light microscopic analysis of the degeneration. In two cases, rats received i o n t o p h o retic applications of horseradish p e r o x i d a s e (50% in water) in the VB and in the s o m a t o s e n s o r y cortex, respectively. In these two cases, non-osmicated sections were submitted to M e s u l a m ' s H R P histochemical technique 9 using 3 , 3 ' , 5 , 5 ' - t e t r a m e t h y l b e n z i d i n e as a c h r o m o g e n , before final mounting and counterstaining with carmine. Out of the 15 rats, 7 were discarded because the diffusion of K A led to a neuronal loss not only in R T but also in VB. In general, injections larger than 0.1 /~l over 20 min ( a p p r o x i m a t e l y 3 nmol of K A ) diffused to VB and rapid injections, even of the lowest quantity, also led to a large lesion. Survival time
seemed to have little influence upon the extent of the lesion. Indeed, as shown in Fig. 1, 10 days after the injection, degeneration could be restricted to R T which is then completely filled with reactive glial cells while VB exhibit apparently normal neurons. These data are in agreement with those of Peterson and Moore is who pointed out the selective effects of K A on diencephalic neurons, especially in RT. H o w e v e r , using striatal injection sites, little if any d e g e n e r a t i o n was observed in other ventral thalamic structures (zona incerta, subthalamus and ventral lateral geniculate nucleus) which were destroyed after more caudal injections. Cortico-thalamic and thalamo-cortical pathways cross the R T and the lack of a lesion of both these pathways was checked using control injections of horseradish peroxidase. They confirmed that cortical and VB neurons could be retrogradely filled after in-
Fig. 4. Electron photomicrograph (24.700 ×) of a degenerated terminal with relative preservation of the membranes bordering a synaptic cleft (arrow). At the bottom left, the inset shows a higher magnification photomicrograph (47,500 x) of the same synaptic arrangement. Note the presence of a densification of the postsynaptic membrane without a postsynaptic density and the existence of numerous swollen vesicles in the electron-dense cytoplasm of the degenerating terminal. Survival time, 1 day.
328 jections in VB and in the somatosensory cortex respectively; in contrast, no R T neurons were labeled after VB injection. Tissue from the 8 remaining animals was studied with the electron microscope and degenerating profiles were found in 5 animals which had survived 24-72 h after injection. The 3 others had survived longer times (5, 7 and 10 days) and did not show degenerating terminal profiles. In the first 5 rats, degenerating myelinated axons (Fig. 2) and terminal profiles (Figs. 3 and 4) were observed throughout the VB. These latter appeared as shrunken terminals with a very irregular outline and were filled with electron dense cytoplasm. Although in such electron dense terminals vesicles are generally swollen and their shape cannot be recognized, several lines of evidence indicate that these terminals are mostly Ftypes: for example the synaptic contact, when preserved, did not exhibit a post-synaptic density (Fig. 4 arrowhead) which indicates a symmetrical (Graytype II) synapse, typical of F type terminals in the rat VB. Degenerating terminals were observed in contact with both large (Fig. 3, bottom right) and thin (Fig. 4) dendrites as well as with somas. Such a widespread variation of contacts is also typical of F-type terminals in the rat VBS,8, ~4. Lastly, no normal F terminals could be seen in the survey of tissue from the 3 animals which survived more than 3 days after the injection. This can be interpreted as the result of the elimination of the degenerated profiles through macrophagic activity. The results of the present study, based on the specific neurotoxic lesion of R T by kainic acid injection indicate that F terminals are associated in the VB with afferents from RT. These results are in agreement with those obtained from studying degenerating terminals in the dorsal lateral geniculate nu-
cleus after either an electrolytic lesion of the R T area 13 or labeled profiles after injection of tritiated amino acid in R T u. A notable point of difference in these studies is the observation that in VB terminals making symmetrical synapses seem to depend completely of R T axons while in the geniculate nucleus, terminals containing pleiomorphic vesicles have been identified 6 which are not labeled after RT lesion or injection. This difference is, however, in agreement with the hypothesis that these 'pleiomorphic' terminals depend on intrinsic (Golgi-type II) neurons since such neurons have been described in the geniculate nucleus (see Discussion in ref. 11) but not in the VB of the rat4,~6,is. Such a similarity in ultrastructural morphology was expected, due to the striking homogeneity exhibited by R T neurons. Indeed all studies of R T neurons indicate that these neurons all project from R T to diencephalic and tectal structures 3, that they exert a comparable inhibitory action upon the various thalamic units ~9 and that they all contain G A B A a and somatostatin 12.
1 Albe-Fessard, D., Stutinski, F. and Libouban, S., Atlas stOr(otaxique du dienc~phale du rat blanc, C NRS, Paris, 1966. 2 Houser, C. R., Vaughn, J. E., Barber, R. P. and Roberts, E., GABA neurons are the major cell type of the nucleus cell type of the nucleus reticularis thalami, Brain Research, 200 (1980) 341-354. 3 Jones, E. G., Some aspects of the organization of the thalamic reticular complex. J. comp. Neurol., 162 (1975) 285-308. 4 Lee, C. L., The Structural Organization of the Rat Ventro-
basal Complex, PhD. Thesis , Univ. California, Berkeley,
The present results are interesting in that they demonstrate at the ultrastructural level that it is possible to destroy an entire synaptic population and thus to disrupt totally the effects exerted by R T neurons upon thalamic neuronal functioning. The effects on G A B A and somatostatin concentrations of such a disruption and the electrophysiological consequences on the VB neuronal activity are presently under study. The authors are greatly indebted to Dr. D. D. Ralston for the review of the manuscript and to Miss Hoch for secretarial assistance. They also wish to thank the members of the SCN 18 of I N S E R M (Dr. Bouteille) for their skillful technical assistance.
1981. 5 Lee, C. L., Peschanski, M. and Ralston, H. J. III, Morphophysiology of neurons of the rat ventrobasal thalamic complex. An intracellular HRP study, Pain, Suppl. 1 (1981) S 210. 6 Lenkov, D. N., Winkelmann, E., Braver, K. and Bruckner, G., Vesicle size in basic classes of synapses in the rat's lateral geniculate nucleus, J. Hirnforsch., 19 (1978) 415-42l. 7 Lieberman, A. R. and Webster, K. E., Aspects of the syn-
329
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11
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13
aptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. An u[trastructural study of the normal and of the experimentally deafferented nucleus of the rat. J. Neurophvsiol., 3 (1911) 677-710. MacAllister. J. P. and Wells, J.. The structural organization of the ventral posterolateral nucleus in the rat, J. comp. Neurol.. i97 ( 1981 ) 271-301. Mesulam. M. M., Tetramethyl benzidine for horseradish peroxidase neurohistochemistry. A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and effcrents, J. Histochem. Cytochem., 26 (1978) 106-117. Minderhood, J. M., An anatomical study of the efferent connections of the thalamic reticular nucleus, Exp. Brain Res.. 12 (1971) 435-446. Montero. V. M. and Scott, G. L., Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study, Neuroscience, 6 (1981) 2561-2578. Oertel, W., Graybiel, A. M,, Mugnaini, E., Elde, R., Schmechel, D. and Kopin. I., Coexistence of glutamate decarboxylase immunoreactivity and somatostatin-like immunoreactivity in neurons of nucleus reticularis thalami of the cat, Neurosci., Abstr., 7 (1981) 223. Ohara, P. T., Sefton. A. J. and Lieberman, A. R., Mode of
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termination of afferents from the thalamic reticular nucleus of the rat, Brain Research, 197, (1980) 503-506. Peschanski, M., Lee, C. L. and Ralston, H. J. Ill, Neurons of the rat ventrobasal thalamic complex responsive to stimuli applied to the face or to the limbs. An intracellular HRP study with electron microscopy, Neurosci. Lett., Suppl. 7 (1981) S 136. Peterson, G. M. and Moore, R. Y., Selective effects of kainic acid on diencephalic neurons, Brain Research, 202 (1980) 165-182. Ralston, H. J. llI, The neuronal and synaptic organization of the ventrobasal thalamus in rat, cat and monkey. In G. Macchi (Ed.), The Somatosensory Thalamus, Elsevier, Amsterdam, in press. Tripp, L. N. and Wells, J., Formation of new synaptic terminals in the somatosensory thalamus of the rat after lesions of the dorsal column nuclei, Brain Research, 155 (1978) 362-367. Wells, J., Mathews, T. J. and Ariano, M A., Are there interneurons in the thalamic somatosensory projection nucleus in the rat?, Soc. Neurosci. Abstr., 8 (1982) 37. Yingling, C. D. and Skinner, J. E., Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami, Electroenceph. clin. Neurophysiol., 41 (1976)476-482.